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Paleoecology and radiocarbon dating of the Pleistocene megafauna of the Brazilian Intertropical Region
Quaternary Research 79 (2013) 61–65
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Paleoecology and radiocarbon dating of the Pleistocene megafauna of the Brazilian Intertropical Region Mário André Trindade Dantas a, b,⁎, Rodrigo Parisi Dutra a, b, Alexander Cherkinsky c, Daniel Costa Fortier b, Luciana Hiromi Yoshino Kamino d, Mario Alberto Cozzuol b, Adauto de Souza Ribeiro e, Fabiana Silva Vieira e a Programa de Pós-graduação em Ecologia, Conservação e Manejo da Vida Silvestre, Av. Antônio Carlos, 6627, CEP 31270-010, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil b Laboratório de Paleozoologia, Departamento de Biologia Geral, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, CEP 31270-010, Belo Horizonte, MG, Brazil c Center for Applied Isotope Studies, University of Georgia, Athens, GA 30602, USA d Programa de Pós-Graduação em Biologia Vegetal, Departamento de Botânica, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, CEP 31270-010, Belo Horizonte, MG, Brazil e Departamento de Biologia, Centro de Ciências Biológicas e da Saúde, Universidade Federal de Sergipe, Av Marechal Rondon s/n, Bairro Rosa Elze, CEP 49100-000, São Cristovão, SE, Brazil
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Article history: Received 8 April 2012 Available online 23 October 2012 Keywords: Megafauna Brazilian Intertropical Region Carbon isotopes AMS
a b s t r a c t During the Pleistocene a fauna composed of large (biomass>44 kg) and giant mammals (biomass>1000 kg) that are usually associated with open environments lived in the Brazilian Intertropical Region. We present here new information concerning the paleoecology and chronology of some species of this megafauna. Carbon isotope analyses were performed for a better understanding of the paleoecology of the species Eremotherium laurillardi (Lund, 1842), Notiomastodon platensis (Ameghino, 1888) and Toxodon platensis (Owen, 1849). The δ13C data allow attributing a generalist diet to these species, which varied according to the kind of habitat in which they lived. In more open habitats all species were grazers; in mixed habitats E. laurillardi and T. platensis were mixed feeders, and N. platensis was grazer; and in more closed habitats all species were mixed feeders. © 2012 University of Washington. Published by Elsevier Inc. All rights reserved.
Introduction The Brazilian Intertropical Region (BIR: sensu Cartelle, 1999) is characterized by the presence of several endemic giant mammals, which lived during the end of the Pleistocene and beginning of the Holocene. The BIR includes all states of the northeastern Brazil (except Maranhão) as well as Goiás, Minas Gerais, Espírito Santo and Rio de Janeiro states (Fig. 1). According to Cartelle (1999), some species from the southern regions of the continent (allochthonous fauna) would have migrated to the BIR at the end of the Pleistocene and beginning of the Holocene. In the BIR, these species would have coexisted sympatrically with the autochthonous fauna of this region, which was adapted to live in dry forests (savannah or steppic savannah). However, chronological data gathered by Dantas et al. (2011) suggested that this fauna was not restricted to the end of the Pleistocene as previously considered and, therefore, they questioned the traditional interpretation regarding the paleoecology of these faunas. The main purpose of the present contribution is to show and to discuss stable carbon isotope and radiocarbon data for Eremotherium laurillardi (Lund, 1842), Notiomastodon platensis ⁎ Corresponding author at: Programa de Pós-graduação em Ecologia, Conservação e Manejo da Vida Silvestre, Av. Antônio Carlos, 6627, CEP 31270-010, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil. E-mail address: [email protected] (M.A.T. Dantas).
(Ameghino, 1888) (=Stegomastodon waringi; Mothé et al., in press) and Toxodon platensis (Owen, 1849) from some localities of the BIR.
Materials and methods Sixteen skeletal samples of Eremotherium laurilardi, N. platensis, and T. platensis from localities in Bahia (BA), Sergipe (SE) and Rio Grande do Norte (RN) (Table 1) were measured to obtain the carbon isotopic composition of bone, dentin and enamel carbonate. Some of these samples (Table 1) were dated using accelerator mass spectrometry (AMS) at the Center for Applied Isotope Studies of the University of Georgia/ USA, calibrated using IntCal98 (Reimer et al., 2009). Samples were collected from fossil specimens housed at the following institutions: Laboratório de Geologia/Universidade Estadual do Sudoeste da Bahia (Bahia, Brazil); Laboratório de Paleontologia/Universidade Federal de Sergipe (Sergipe, Brazil); Memorial de Sergipe/Universidade Tiradentes (Sergipe, Brazil); and Museu Câmara Cascudo/Universidade Federal do Rio Grande do Norte (Rio Grande do Norte, Brazil). Data from the 13C analyses (δ 13C ‰) were used to infer the diet of the studied mammals. In medium- to large-sized animals δ 13C can be enriched by 12‰ to 14‰ (Cerling and Harris, 1999). Values of δ13C b −10‰, which were found in the tooth enamel, represent a pure C3 feeder, whereas values of δ13C >−1‰ represent a diet based on C4 grasses. Values of δ13C between −10‰ and −1‰ indicate a mixed
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Figure 1. Brazilian Intertropical Region (BIR) map, showing the potencial distribution of the Atlantic Forest (modified from Carnaval and Moritz, 2008) and the Dry Tropical Forest (after Werneck et al., 2011). (A) Represents a region which includes the municipalities of: Vitória da Conquista/BA, Morro do Chapéu/BA, Ourolândia/BA, Quinjingue/BA, and, tentatively, Toca do Gordo do Garrincho/PI (?), Águas de Araxá/MG (?) and São José do Itaboraí/RJ (?). (B) Region that includes the municipalities of Coronel João Sá/BA, Poço Redondo/SE, Gararu/SE, Canhoba/SE and Maravilha/AL. (C) Region that includes the municipalities of Rui Barbosa/RN, Barcelona/RN and Currais Novos/RN. States that comprise the BIR: GO — Góias; MG — Minas Gerais; RJ — Rio de Janeiro; ES — Espirito Santo; BA — Bahia; SE — Sergipe; AL — Alagoas; PE — Pernambuco; PB — Paraíba; RN — Rio Grande do Norte; CE — Ceará; PI — Piauí (sensu Cartelle, 1999).
diet of C3 and C4 plants (MacFadden et al., 1999; MacFadden, 2005). These values were here considered in the interpretation of isotopes values for both bone and dentin. Examples of recent studies with this
approach were conducted by MacFadden et al. (1999) for Equus; Sánchez et al. (2004) for Notiomastodon and Cuvieronious; and MacFadden (2005) for Toxodon and Mixotoxodon.
Table 1 13 C analyses and radiocarbon dating for skeletal elements of Brazilian Intertropical Region fossils. Legends — skeletal tissue (st): d (dentine); b (bone); or e (enamel). Species Eremotherium laurillardi Eremotherium laurillardi Eremotherium laurillardi Eremotherium laurillardi Eremotherium laurillardi Eremotherium laurillardi Eremotherium laurillardi Eremotherium laurillardi Eremotherium laurillardi Notiomastodon platensis Notiomastodon platensis Notiomastodon platensis Notiomastodon platensis Notiomastodon platensis Notiomastodon platensis Notiomastodon platensis Notiomastodon platensis Notiomastodon platensis Toxodon platensis Toxodon platensis Toxodon platensis Toxodon platensis Toxodon platensis Toxodon platensis Toxodon platensis Toxodon platensis Toxodon platensis Toxodon platensis
Sample number (3)
UGAMS 4935 UGAMS 4936(3) SM-1(1) MA-1(1) UGAMS 4931(3) UGAMS 4932(3) UGAMS 4933(3) UGAMS 4934(3) UGAMS 6136(2) UGAMS 4940(3) SM-3(1) MA-3(1) UGAMS 4937(3) UGAMS 4938(3) UGAMS 4939(3) UGAMS 4941(3) s/n(4) s/n(4) UGAMS 4942(3) SM-5(1) MA-5(1) UGAMS 4946(3) UGAMS 4943(3) UGAMS 4944(3) U-96-150(5) U-96-148(5) U-96-149(5) UGAMS 4944(3)
Localities (A)
Currais Novos/RN Barcelona/RN(A) Maravilha/AL Maravilha/AL Poço Redondo/SE(B) Poço Redondo/SE(B) Poço Redondo/SE(B) Gararu/SE(B) Quijingue/BA Barcelona/RN(A) Maravilha/AL Maravilha/AL Poço Redondo/SE(B) Cel. João Sá/BA(B) Canhoba/SE(C) Cel. João Sá/BA(B) Ourolândia/BA Ourolândia/BA Rui Barbosa/RN(A) Maravilha/AL Maravilha/AL Poço Redondo/SE(B) Cel. João Sá/BA(B) Cel. João Sá/BA(B) Pedra Vermelha/BA Ourolândia/BA Ourolândia/BA Vitória da Conquista/BA(D)
Lat (°S)
δ13C (‰) on st
14
C age ±1σ on st (14C yr BP)
6 6 9 9 9 9 9 10 10 6 9 9 10 10 10 10 10 10 6 9 9 9 10 10 10 10 10 14
0.50 (d) 5.22 (d) 0.30 (d) −12.00 (d) −6.65 (d) −3.85 (d) −2.45 (d) −3.25 (d) −18.20 (b) 0.44 (e) 0.00 (d) 1.47 (d) 0.76 (e) −1.04 (e) −1.86 (e) −0.49 (e) −8.20 (e) −5.00 (e) −1.32 (e) −4.10 (d) 1.51 (d) −3.68 (e) −1.08 (e) −1.00 (e) −5.50 (e) −12.60 (e) −7.70 (e) −13.24 (e)
15,490 ± 40 – – – – 22,440 ± 50 – – 15,770 ± 40 16,150 ± 40 – – – 13,980 ± 40 17,910 ± 50 – – – 10,730 ± 30 – – 10,050 ± 30 – – – – – 10,970 ± 30
(b)
(d)
(b) (e)
(e) (e)
(e)
(e)
(e)
Calibrated age⁎ (2σ range, cal yr BP) 18,580–18,850 – – – – 26,690–27,690 – – 18,730–19,280 18,930–19,450 – – – 16,800–17,380 21,180–21,550 – – – 12,560–12,720 – – 11,400–11,750 – – – – – 12,660–13,050
⁎Calibrated with IntCal98 (Reimer et al., 2009) and calculated with Calib 6.0 (http://calib.qub.ac.uk/calib/calib.html; last accessed 25 September 2012). (1) Silva (2009); (2)Drefahl (2010); (3)Our data; (4)Sánchez et al. (2004); (5)MacFadden (2005) Institutions. (A)Museu Câmara Cascudo/Universidade Federal do Rio Grande do Norte; (B)Laboratório de Paleontologia/Universidade Federal de Sergipe; (C)Memorial de Sergipe/Universidade Tiradentes; (D)Laboratório de Geologia/Universidade Estadual do Sudoeste da Bahia.
M.A.T. Dantas et al. / Quaternary Research 79 (2013) 61–65
Results Paleoecology E. laurillardi δ13C values found in the dentin of the fossil teeth from Sergipe display a variation between −6.65‰ and −2.45‰ (Table 1). This range indicates that this species probably had a generalist diet, consuming C3 and C4 plants (MacFadden et al., 1999; MacFadden, 2005). Even more negative values were found in the specimens collected in Alagoas (δ 13C = −12.00‰: Silva, 2009) and Bahia (δ 13C = −18.20‰: Drefahl, 2010) states, but they indicate an exclusive diet of C3 plants. The data collected from E. laurillardi fossils, of the Rio Grande do Norte state, showed that this species also had a C4 plant diet (δ13C = 0.50‰ and 5.22‰). Similar values were found by Viana et al. (2011) in fossil material from Alagoas (δ13C = 0.30‰). Although the dental morphology of this species precludes grazing, Bargo et al. (2006) observed that Megatherium americanum and probably E. laurillardi as well, presented a high capability of oral processing and a strong bite. The former feature could suggest a low digestive efficiency and the latter would allow feeding on material ranging from moderate to soft consistency, similar to what is found in leaves and some fruits. An omnivore diet for Megatheriines (M. americanum) was proposed by Fariña (1996), but the hypothesis was never tested. N. platensis The specimens from the north of Bahia, Sergipe and Rio Grande do Norte showed similar values of δ13C in tooth enamel, varying between −1.86‰ and 0.76‰ (Table 1). Similar values were found in fossil material from Alagoas, in which δ 13C = 0.00‰ and 1.47‰ (Silva, 2009; Viana et al., 2011), indicating a diet comprised of C4 grasses. However, a generalist diet (C3 and C4 plants; δ 13C = −8.20‰ and −5.00‰) was also attributed to mastodonts found in the central part of Bahia by Sánchez et al. (2004). This type of diet was suggested by Guimarães et al. (2008) as well, and confirmed by Asevedo et al. (2011a,b), who based their analysis on teeth microwear and tooth calculus obtained from the fossil material of the Toca do Gordo do Garrincho, Piauí (PI); Águas do Araxá, Minas Gerais (MG) and São José do Itaboraí, Rio de Janeiro (RJ). T. platensis In the analyses of carbon isotopes for this species, δ13C values ranging from −3.68‰ to −1.00‰ (Table 1) were found in the material from the north of Bahia, Rio Grande do Norte and Sergipe. Similar values were obtained by Silva (2009) and Viana et al. (2011) when they worked with material from Alagoas (δ13C = −4.10‰ to 1.51‰). These values indicate a diet based on C4 grasses. However, more negative values were obtained in our analyses of the remains from the south of Bahia (δ 13C = −13.24‰), similar to the values presented by MacFadden (2005) for fossil material collected in Ourolândia, northeastern Bahia (δ 13C = −12.60‰ and −7.70‰) and Pedra Vermelha, in the north of Bahia state (δ13C = −5.50‰). These results indicate that this species had a mixed diet as well (C3 and C4 plants).
2010, Table 1). The compilation of these dates reveals that this species lived in the BIR during the upper Pleistocene, 27–15 ka (Table 2). The age assigned to the N. platensis samples (Table 1) varied from 16,800–17,380 cal yr BP (13,980 ± 40 14C yr BP, UGAMS 4938) to 21,180–21,550 cal yr BP (17,910 ± 50 14C yr BP, UGAMS 4939). This is the species for which the largest number of specimens was previously dated (Table 2). Our results confirm the occurrence of this species between 17 ka and 22 ka. When the results of all published dates are combined, the occurrence of this species is estimated between 71 ka and 10 ka (Table 2). The ages assigned to the material of T. platensis (Table 1) ranged between 11,400–11,750 cal yr BP (10,050±30 14C yr BP, UGAMS 4946) and 12,660–13,050 cal yr BP (10,970±30 14C yr BP, UGAMS 4944). These ages reinforce the occurrence of this species in the beginning of the Holocene in the BIR as shown by Ribeiro et al. (in press; Table 2). These results combined with others from previous dating analyses indicate the occurrence of this species between 50 ka and 9 ka (Dantas et al., 2011; Ribeiro et al., in press; Table 2). Discussion Available chronological data (e.g. Auler et al., 2006; Dantas et al., 2011; Ribeiro et al., in press) indicated that E. laurillardi, N. platensis and T. platensis were present in the BIR during a long period of humidity at the end of the Pleistocene, between 40 ka and 10 ka. During this period the rainforests expanded (Behling et al., 2000; Auler and Smart, 2001; Sifeddine et al., 2003; Barreto, 2010), possibly providing a connection between the Atlantic forest and the Amazon rainforest. Although some pollen data for the dry forests (e.g. De Oliveira et al., 1999) and fossil leaves for the Atlantic forest of the BIR (e.g. Souza-Lima and Farias, 2008) pointed to a Pleistocene age, it is uncertain how these biomes were distributed in the BIR during the end of the Pleistocene. Due to this uncertainty, maps of potential distribution of the Atlantic forest (Carnaval and Moritz, 2008) and of the dry forests (savannah or steppic savannah; Werneck et al., 2011) comprising a period of 21 ka (Fig. 1) were used in order to observe the distribution of the studied fauna in relation to the biomes. We verified that the studied taxa were present both in open and closed environments. The resulting 13C data were grouped into three sub-regions: A (Rio Grande do Norte); B (Alagoas, Sergipe and north of Bahia); and C (south of Bahia). We considered that these species had the same diet in open environments, while in closed environments they showed differences, ranging from mixed feeders to exclusive C3 plants feeders (Table 1; Fig. 2). With regard to the 13C data, both ANOVA (E. laurillardi, Fobs =16.11, P=0.0029; N. platensis, Fobs =19.60, P=0.0018; T. platensis, Fobs = 10.77, P=0.0058) and non-parametric Kruskal–Wallis tests (E. laurillardi, Hobs =7.02, P=0.0298; T. platensis, Hobs =7.09, P=0.0288) indicate
Table 2 Compilation of the geochronological data for the species Eremotherium laurillardi, Notiomastodon platensis and Toxodon platensis found in fossiliferous deposits (“tanks” and caves) in the Brazilian Intertropical Region. Species
Age, ka 10−15 15−20 20−25 25−30 30−35 35−40 40−45 45−50 50−55 55−60 60−65
Radiocarbon dating The 14C dating analyses were performed using AMS for the E. laurillardi samples (Table 1) from the municipalities of Poço Redondo/SE and Currais Novos/RN. The results were, respectively, 26,690–27,690 cal yr BP (22,240 ± 50 14C yr BP, UGAMS 4932) and 18,580–18,850 cal yr BP (15,490 ±40 14C yr BP, UGAMS 4935). The age assigned for the sample of Sergipe state is the oldest reported for this species, whereas the age assigned to the material from Rio Grande do Norte is similar to the age obtained in two previous analyses using different techniques (Auler et al., 2006, U 238/Th230, 15 ka; Drefahl,
63
(1,2,3)
E. laurillardi
N. platensis
(4)
T. platensis
(3, 8, 9)
(1)
(3)
(3)
(3)
(5)
(5,6)
(4)
(8)
(6)
(7)
(6)
Auler et al. (2006), (2)Drefahl (2010), (3)Our data, (4)Oliveira et al. (2010), Kinoshita et al. (2005), (6)Dantas et al. (2011), (7)Kinoshita et al. (2008), (8) Ribeiro et al. (in press), (9)Neves et al. (2007). (5)
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both dental microwear analyses and tooth calculus suggested that N. platensis had the same type of diet, revealing that the same environmental conditions were present at the localities of Toca do Gordo do Garrincho/PI, Água de Araxá/MG, and São José do Itaboraí/RJ (Fig. 1). Conclusions
Figure 2. Tooth enamel carbon isotope (13C) values for the species analyzed in this study.
statistically significant differences among the three geographic samples. The only exception was the Kruskal–Wallis tests for N. platensis which indicated the same diet in all sub-regions. Between the latitudes 6°S to 9°S, there is a wide area (sub-region A, Fig. 1) in which the dry forests seemed to be predominant, most probably Caatinga vegetation (Behling et al., 2000; Werneck et al., 2011). The material concerning the three species which were collected in Rio Grande do Norte gives δ13C values that indicate a diet based exclusively on C4 grasses (Table 1). It is possible that in this kind of environment these species had a high competition for resources since they shared similar niches. South of latitude 9°S, in the region of Alagoas, Sergipe and northern of Bahia (sub-region B, Fig. 1), N. platensis had the same diet based exclusively on C4 grasses, which indicates that this was perhaps its predominant diet (Table 1), while E. laurillardi and T. platensis stopped feeding exclusively on C4 grasses and start browsing on C3 plants, thus becoming generalists (Table 1). The exclusive C3 plant-feeder value found in a sample from Alagoas for E. laurillardi (δ13C = −12.00‰, Silva, 2009) can be explained as a migrant specimen which came from Bahia. We infer that these C3 values are not from grasses, because a similar isotopic signal of C3 grass and browse plants occurs only at high latitudes (>35°S) or at high elevations (>3000 m) (MacFadden, 2005), which are not characteristic of our area of study. The vegetation in this region (sub-region B, Fig. 1) during this period is interpreted as a mosaic of dry forests (steppic savannah) and rainforests (Atlantic forest), where the species could occupy different niches and consequently reduce the competition for resources. In most of Bahia state (except for the northern region), and perhaps Minas Gerais, Piauí and Rio de Janeiro states, there would be the predominance of the Atlantic forest (Sub-region C, Fig. 1; Carnaval and Moritz, 2008), comprising a more closed area than found between latitudes 6°S and 10°S. Drefahl (2010) presented 13C data concerning E. laurillardi (Table 1) in this region, suggesting that in closed environments the diet of this species consisted exclusively in C3 plants. The fruits would be one of its main sources of food, thus the taxon is pointed as one of the main dispersal vectors of different botanic species (Guimarães et al., 2008). The data available for T. platensis and N. platensis pointed that in more closed environments these species fed more in C3 brows plant than in C4 grasses, tending to be exclusive C3 plant feeder (Table 1). Other evidence also supports this hypothesis. For example, the 13C data indicate the same type of diet for the fossil material related to these species. The material was found in a forest environment of the Amazon basin and its age ranged from 38.5 to 15 ka (Rossetti et al., 2004; MacFadden, 2005). Besides, Asevedo et al. (2011a,b) through
The fauna composed of the populations of E. laurillardi, N. platensis and T. platensis shows different diets throughout the Brazilian Intertropical Region, varying from exclusively grass feeders to mixed feeders. Thus, this fauna should not be used as an indicator of open environments, as Rossetti et al. (2004) previously stated. In a more closed environment these species tended to feed more on C3 plants, while in open area environments these species fed on C4 plants. In the latter, these species probably had a major competition for resources, which led them to have a population below its ideal number. Based on the carbon isotopic analysis, we considered that the ideal habitat for these species to be a mixed environment of Atlantic and dry tropical forest, since they presented different kinds of diet, which should decrease the competition for resources, and, maybe, allowed them to reach the ideal number of individuals for its populations. Acknowledgment We thank CAPES for the doutorament (doctoral) scholarship given to the first author, and FAPEMIG and USFISH for resources that helped with fields and the analysis. We thank Priscila Torres and Ale Boss for the English review of the manuscript, Adriana Bocchiglieri for the help in the statistical analyses, and anonymous reviewers whose corrections and suggestions improved the quality of this manuscript. References Asevedo, L., Winck, G.R., Mothé, D., Avilla, L.S., 2011a. Ancient diet of the Pleistocene gomphothere Notiomastodon platensis (Mammalia, Proboscidea, Gomphotheriidae) from lowland mid-latitudes of South America: stereomicrowear and tooth calculus analyses combined. Quaternary International http://dx.doi.org/10.1016/j.quaint. 2011.08.037. Asevedo, L., Oliveira, G.F. de, Avilla, L.S., Oliveira, E., Mothé, D., Winck, G.R., 2011b. Reconstrução da paleodieta de Notiomastodon platensis (Gomphotheriidae: Proboscidea: Mammalia) via análises de microdesgaste e cálculo dentário. Boletim de Resumos, Paleo2011, Alegre, Espírito Santo. Auler, A.S., Smart, P.L., 2001. Late Quaternary paleoclimate in semiarid northeastern Brazil from U-series dating of travertine and water-table speleothems. Quaternary Research 55, 159–167 http://dx.doi.org/10.1006/qres.2000.2213. Auler, A.S., Piló, L.B., Smart, P.L., Wang, X., Hoffmann, D., Richards, D.A., Edwards, R.L., Neves, W.A., Cheng, H., 2006. U-series dating and taphonomy of Quaternary vertebrates from Brazilian caves. Palaeogeography, Palaeoclimatology, Palaeoecology 240, 508–522 http://dx.doi.org/10.1016/j.palaeo.2006.03.002. Bargo, M.S., De Iuliis, G., Vizcaíno, S.F., 2006. Hypsodonty in Pleistocene ground sloths. Acta Palaeontolica Polonica 51 (1), 53–61. Barreto, E.A. de S., 2010. Reconstituição da pluviosidade da Chapada Diamantina (BA) durante o Quaternário tardio através de registros isotópicos (O e C) em estalagmites. Programa de Pós-graduação em Geoquímica e Geotectônica, Universidade de São Paulo, Dissertação de Mestrado, 133 pp. Behling, H., Arz, H.W., Tzold, J.R.P., Wefer, G., 2000. Late Quaternary vegetational and climate dynamics in northeastern Brazil, inferences from marine core GeoB 3104-1. Quaternary Science Reviews 19, 981–994. Carnaval, A.C., Moritz, G., 2008. Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic Forest. Journal of Biogeography 35, 1187–1201 http://dx.doi.org/10.1111/j.1365-2699.2007.01870.x. Cartelle, C., 1999. Pleistocene mammals of the Cerrado and Caatinga of Brazil. In: Eisenberg, J.F., Redford, K.H. (Eds.), Mammals of the Neotropics. The University of Chicago Press, pp. 27–46. Cerling, T.E., Harris, J.M., 1999. Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120, 347–363. Dantas, M.A.T., Porpino, K.deO., Bauermann, S.G., Prata, A.P. do N., Cozzuol, M.A., Kinoshita, A., Barbosa, J.H.O., Baffa, O., 2011. Megafauna do Pleistoceno superior de Sergipe, Brasil: registros taxonômicos e cronológicos. Revista Brasileira de Paleontologia 14 (3), 311–320 http://dx.doi.org/10.4072/rbp. 2011.3.10. De Oliveira, P.E., Barreto, A.M.F., Suguio, K., 1999. Late Pleistocene/Holocene climatic and vegetational history of the Brazilian Caatinga: the fossil dunes of the middle São Francisco river. Palaeogeography, Palaeoclimatology, Palaeoecology 152, 319–337.
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Reimer, P.J., Baillie, M.G.L., Bard, E., et al., 2009. IntCal09 and Marine09: radiocarbon age calibration curves, 0–50,000 years cal BP. Radiocarbon 51 (4), 1111–1150. Ribeiro, R. Da C., Kinoshita, A., Figueiredo, A.M.G., Carvalho, I. de S., Baffa, O., in press. Electron spin resonance dating of the late Quaternary megafauna fossils from Baixa Grande, Bahia, Brazil. Quaternary International http://dx.doi.org/10.1016/j.quaint. 2012.07.017. Rossetti, D.deF., Toledo, P.M. de, Moraes-Santos, H.M., Santos Jr., A.M.de A., 2004. Reconstructing habitats in central Amazonia using megafauna, sedimentology, radiocarbon, and isotope analyses. Quaternary Research 61, 289–300 http:// dx.doi.org/10.1016/j.yqres.2004.02.010. Sánchez, B., Prado, J.L., Alberdi, M.T., 2004. Feeding ecology, dispersal, and extinction of South American Pleistocene gomphotheres (Gomphotheriidae, Proboscidea). Paleobiology 30 (1), 146–161. Sifeddine, A., Albuquerque, A.L.S., Ledru, M.-P.L., Turcq, B., Knoppers, B., Martin, L., Mello, W.Z., Passenau, H., Dominguez, J.M.L., Cordeiro, R.C., Abrão, J.J., Bittencourt, A.C.S.P., 2003. A 21,000 cal years paleoclimatic record from Caço Lake, Northern, Brazil: evidence from sedimentary and pollen analyses. Palaeogeography, Palaeoclimatology, Palaeoecology 189, 25–34. Silva, J.L.L. da, 2009. Reconstituição paleoambiental baseada no estudo de mamíferos pleistocênicos de Maravilha e Poço das Trincheiras, Alagoas, nordeste do Brasil. 244 pp. Tese de Doutorado — Curso de Pós Graduação em Geociências, Universidade Federal de Pernambuco, Recife. Souza-Lima, W., Farias, R.M., 2008. A flora Quaternária dos travertinos da região de Itabaiana, Sergipe. Palaeontologia em Destaque 23 (61), 9. Viana, M.S.S., da Silva, J.L.L., de Oliveira, P.V.daS., Julião, M.S., 2011. Hábitos alimentares em herbívoros da megafauna pleistocênica do Nordeste do Brasil. Estudos Geológicos 21 (2), 89–95. Werneck, F.P., Costa, G.C., Colli, G.R., Prado, D.E., Sites Jr., J.W., 2011. Revisiting the historical distribution of seasonally dry tropical forests: new insights based on palaeodistribution modelling and palynological evidence. Global Ecology and Biogeography 20, 272–288 http://dx.doi.org/10.1111/j.1466-8238.2010. 00596.x.
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Paleoecology and radiocarbon dating of the Pleistocene megafauna of the Brazilian Intertropical Region Mário André Trindade Dantas a, b,⁎, Rodrigo Parisi Dutra a, b, Alexander Cherkinsky c, Daniel Costa Fortier b, Luciana Hiromi Yoshino Kamino d, Mario Alberto Cozzuol b, Adauto de Souza Ribeiro e, Fabiana Silva Vieira e a Programa de Pós-graduação em Ecologia, Conservação e Manejo da Vida Silvestre, Av. Antônio Carlos, 6627, CEP 31270-010, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil b Laboratório de Paleozoologia, Departamento de Biologia Geral, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, CEP 31270-010, Belo Horizonte, MG, Brazil c Center for Applied Isotope Studies, University of Georgia, Athens, GA 30602, USA d Programa de Pós-Graduação em Biologia Vegetal, Departamento de Botânica, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, CEP 31270-010, Belo Horizonte, MG, Brazil e Departamento de Biologia, Centro de Ciências Biológicas e da Saúde, Universidade Federal de Sergipe, Av Marechal Rondon s/n, Bairro Rosa Elze, CEP 49100-000, São Cristovão, SE, Brazil
a r t i c l e
i n f o
Article history: Received 8 April 2012 Available online 23 October 2012 Keywords: Megafauna Brazilian Intertropical Region Carbon isotopes AMS
a b s t r a c t During the Pleistocene a fauna composed of large (biomass>44 kg) and giant mammals (biomass>1000 kg) that are usually associated with open environments lived in the Brazilian Intertropical Region. We present here new information concerning the paleoecology and chronology of some species of this megafauna. Carbon isotope analyses were performed for a better understanding of the paleoecology of the species Eremotherium laurillardi (Lund, 1842), Notiomastodon platensis (Ameghino, 1888) and Toxodon platensis (Owen, 1849). The δ13C data allow attributing a generalist diet to these species, which varied according to the kind of habitat in which they lived. In more open habitats all species were grazers; in mixed habitats E. laurillardi and T. platensis were mixed feeders, and N. platensis was grazer; and in more closed habitats all species were mixed feeders. © 2012 University of Washington. Published by Elsevier Inc. All rights reserved.
Introduction The Brazilian Intertropical Region (BIR: sensu Cartelle, 1999) is characterized by the presence of several endemic giant mammals, which lived during the end of the Pleistocene and beginning of the Holocene. The BIR includes all states of the northeastern Brazil (except Maranhão) as well as Goiás, Minas Gerais, Espírito Santo and Rio de Janeiro states (Fig. 1). According to Cartelle (1999), some species from the southern regions of the continent (allochthonous fauna) would have migrated to the BIR at the end of the Pleistocene and beginning of the Holocene. In the BIR, these species would have coexisted sympatrically with the autochthonous fauna of this region, which was adapted to live in dry forests (savannah or steppic savannah). However, chronological data gathered by Dantas et al. (2011) suggested that this fauna was not restricted to the end of the Pleistocene as previously considered and, therefore, they questioned the traditional interpretation regarding the paleoecology of these faunas. The main purpose of the present contribution is to show and to discuss stable carbon isotope and radiocarbon data for Eremotherium laurillardi (Lund, 1842), Notiomastodon platensis ⁎ Corresponding author at: Programa de Pós-graduação em Ecologia, Conservação e Manejo da Vida Silvestre, Av. Antônio Carlos, 6627, CEP 31270-010, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil. E-mail address: [email protected] (M.A.T. Dantas).
(Ameghino, 1888) (=Stegomastodon waringi; Mothé et al., in press) and Toxodon platensis (Owen, 1849) from some localities of the BIR.
Materials and methods Sixteen skeletal samples of Eremotherium laurilardi, N. platensis, and T. platensis from localities in Bahia (BA), Sergipe (SE) and Rio Grande do Norte (RN) (Table 1) were measured to obtain the carbon isotopic composition of bone, dentin and enamel carbonate. Some of these samples (Table 1) were dated using accelerator mass spectrometry (AMS) at the Center for Applied Isotope Studies of the University of Georgia/ USA, calibrated using IntCal98 (Reimer et al., 2009). Samples were collected from fossil specimens housed at the following institutions: Laboratório de Geologia/Universidade Estadual do Sudoeste da Bahia (Bahia, Brazil); Laboratório de Paleontologia/Universidade Federal de Sergipe (Sergipe, Brazil); Memorial de Sergipe/Universidade Tiradentes (Sergipe, Brazil); and Museu Câmara Cascudo/Universidade Federal do Rio Grande do Norte (Rio Grande do Norte, Brazil). Data from the 13C analyses (δ 13C ‰) were used to infer the diet of the studied mammals. In medium- to large-sized animals δ 13C can be enriched by 12‰ to 14‰ (Cerling and Harris, 1999). Values of δ13C b −10‰, which were found in the tooth enamel, represent a pure C3 feeder, whereas values of δ13C >−1‰ represent a diet based on C4 grasses. Values of δ13C between −10‰ and −1‰ indicate a mixed
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M.A.T. Dantas et al. / Quaternary Research 79 (2013) 61–65
Figure 1. Brazilian Intertropical Region (BIR) map, showing the potencial distribution of the Atlantic Forest (modified from Carnaval and Moritz, 2008) and the Dry Tropical Forest (after Werneck et al., 2011). (A) Represents a region which includes the municipalities of: Vitória da Conquista/BA, Morro do Chapéu/BA, Ourolândia/BA, Quinjingue/BA, and, tentatively, Toca do Gordo do Garrincho/PI (?), Águas de Araxá/MG (?) and São José do Itaboraí/RJ (?). (B) Region that includes the municipalities of Coronel João Sá/BA, Poço Redondo/SE, Gararu/SE, Canhoba/SE and Maravilha/AL. (C) Region that includes the municipalities of Rui Barbosa/RN, Barcelona/RN and Currais Novos/RN. States that comprise the BIR: GO — Góias; MG — Minas Gerais; RJ — Rio de Janeiro; ES — Espirito Santo; BA — Bahia; SE — Sergipe; AL — Alagoas; PE — Pernambuco; PB — Paraíba; RN — Rio Grande do Norte; CE — Ceará; PI — Piauí (sensu Cartelle, 1999).
diet of C3 and C4 plants (MacFadden et al., 1999; MacFadden, 2005). These values were here considered in the interpretation of isotopes values for both bone and dentin. Examples of recent studies with this
approach were conducted by MacFadden et al. (1999) for Equus; Sánchez et al. (2004) for Notiomastodon and Cuvieronious; and MacFadden (2005) for Toxodon and Mixotoxodon.
Table 1 13 C analyses and radiocarbon dating for skeletal elements of Brazilian Intertropical Region fossils. Legends — skeletal tissue (st): d (dentine); b (bone); or e (enamel). Species Eremotherium laurillardi Eremotherium laurillardi Eremotherium laurillardi Eremotherium laurillardi Eremotherium laurillardi Eremotherium laurillardi Eremotherium laurillardi Eremotherium laurillardi Eremotherium laurillardi Notiomastodon platensis Notiomastodon platensis Notiomastodon platensis Notiomastodon platensis Notiomastodon platensis Notiomastodon platensis Notiomastodon platensis Notiomastodon platensis Notiomastodon platensis Toxodon platensis Toxodon platensis Toxodon platensis Toxodon platensis Toxodon platensis Toxodon platensis Toxodon platensis Toxodon platensis Toxodon platensis Toxodon platensis
Sample number (3)
UGAMS 4935 UGAMS 4936(3) SM-1(1) MA-1(1) UGAMS 4931(3) UGAMS 4932(3) UGAMS 4933(3) UGAMS 4934(3) UGAMS 6136(2) UGAMS 4940(3) SM-3(1) MA-3(1) UGAMS 4937(3) UGAMS 4938(3) UGAMS 4939(3) UGAMS 4941(3) s/n(4) s/n(4) UGAMS 4942(3) SM-5(1) MA-5(1) UGAMS 4946(3) UGAMS 4943(3) UGAMS 4944(3) U-96-150(5) U-96-148(5) U-96-149(5) UGAMS 4944(3)
Localities (A)
Currais Novos/RN Barcelona/RN(A) Maravilha/AL Maravilha/AL Poço Redondo/SE(B) Poço Redondo/SE(B) Poço Redondo/SE(B) Gararu/SE(B) Quijingue/BA Barcelona/RN(A) Maravilha/AL Maravilha/AL Poço Redondo/SE(B) Cel. João Sá/BA(B) Canhoba/SE(C) Cel. João Sá/BA(B) Ourolândia/BA Ourolândia/BA Rui Barbosa/RN(A) Maravilha/AL Maravilha/AL Poço Redondo/SE(B) Cel. João Sá/BA(B) Cel. João Sá/BA(B) Pedra Vermelha/BA Ourolândia/BA Ourolândia/BA Vitória da Conquista/BA(D)
Lat (°S)
δ13C (‰) on st
14
C age ±1σ on st (14C yr BP)
6 6 9 9 9 9 9 10 10 6 9 9 10 10 10 10 10 10 6 9 9 9 10 10 10 10 10 14
0.50 (d) 5.22 (d) 0.30 (d) −12.00 (d) −6.65 (d) −3.85 (d) −2.45 (d) −3.25 (d) −18.20 (b) 0.44 (e) 0.00 (d) 1.47 (d) 0.76 (e) −1.04 (e) −1.86 (e) −0.49 (e) −8.20 (e) −5.00 (e) −1.32 (e) −4.10 (d) 1.51 (d) −3.68 (e) −1.08 (e) −1.00 (e) −5.50 (e) −12.60 (e) −7.70 (e) −13.24 (e)
15,490 ± 40 – – – – 22,440 ± 50 – – 15,770 ± 40 16,150 ± 40 – – – 13,980 ± 40 17,910 ± 50 – – – 10,730 ± 30 – – 10,050 ± 30 – – – – – 10,970 ± 30
(b)
(d)
(b) (e)
(e) (e)
(e)
(e)
(e)
Calibrated age⁎ (2σ range, cal yr BP) 18,580–18,850 – – – – 26,690–27,690 – – 18,730–19,280 18,930–19,450 – – – 16,800–17,380 21,180–21,550 – – – 12,560–12,720 – – 11,400–11,750 – – – – – 12,660–13,050
⁎Calibrated with IntCal98 (Reimer et al., 2009) and calculated with Calib 6.0 (http://calib.qub.ac.uk/calib/calib.html; last accessed 25 September 2012). (1) Silva (2009); (2)Drefahl (2010); (3)Our data; (4)Sánchez et al. (2004); (5)MacFadden (2005) Institutions. (A)Museu Câmara Cascudo/Universidade Federal do Rio Grande do Norte; (B)Laboratório de Paleontologia/Universidade Federal de Sergipe; (C)Memorial de Sergipe/Universidade Tiradentes; (D)Laboratório de Geologia/Universidade Estadual do Sudoeste da Bahia.
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Results Paleoecology E. laurillardi δ13C values found in the dentin of the fossil teeth from Sergipe display a variation between −6.65‰ and −2.45‰ (Table 1). This range indicates that this species probably had a generalist diet, consuming C3 and C4 plants (MacFadden et al., 1999; MacFadden, 2005). Even more negative values were found in the specimens collected in Alagoas (δ 13C = −12.00‰: Silva, 2009) and Bahia (δ 13C = −18.20‰: Drefahl, 2010) states, but they indicate an exclusive diet of C3 plants. The data collected from E. laurillardi fossils, of the Rio Grande do Norte state, showed that this species also had a C4 plant diet (δ13C = 0.50‰ and 5.22‰). Similar values were found by Viana et al. (2011) in fossil material from Alagoas (δ13C = 0.30‰). Although the dental morphology of this species precludes grazing, Bargo et al. (2006) observed that Megatherium americanum and probably E. laurillardi as well, presented a high capability of oral processing and a strong bite. The former feature could suggest a low digestive efficiency and the latter would allow feeding on material ranging from moderate to soft consistency, similar to what is found in leaves and some fruits. An omnivore diet for Megatheriines (M. americanum) was proposed by Fariña (1996), but the hypothesis was never tested. N. platensis The specimens from the north of Bahia, Sergipe and Rio Grande do Norte showed similar values of δ13C in tooth enamel, varying between −1.86‰ and 0.76‰ (Table 1). Similar values were found in fossil material from Alagoas, in which δ 13C = 0.00‰ and 1.47‰ (Silva, 2009; Viana et al., 2011), indicating a diet comprised of C4 grasses. However, a generalist diet (C3 and C4 plants; δ 13C = −8.20‰ and −5.00‰) was also attributed to mastodonts found in the central part of Bahia by Sánchez et al. (2004). This type of diet was suggested by Guimarães et al. (2008) as well, and confirmed by Asevedo et al. (2011a,b), who based their analysis on teeth microwear and tooth calculus obtained from the fossil material of the Toca do Gordo do Garrincho, Piauí (PI); Águas do Araxá, Minas Gerais (MG) and São José do Itaboraí, Rio de Janeiro (RJ). T. platensis In the analyses of carbon isotopes for this species, δ13C values ranging from −3.68‰ to −1.00‰ (Table 1) were found in the material from the north of Bahia, Rio Grande do Norte and Sergipe. Similar values were obtained by Silva (2009) and Viana et al. (2011) when they worked with material from Alagoas (δ13C = −4.10‰ to 1.51‰). These values indicate a diet based on C4 grasses. However, more negative values were obtained in our analyses of the remains from the south of Bahia (δ 13C = −13.24‰), similar to the values presented by MacFadden (2005) for fossil material collected in Ourolândia, northeastern Bahia (δ 13C = −12.60‰ and −7.70‰) and Pedra Vermelha, in the north of Bahia state (δ13C = −5.50‰). These results indicate that this species had a mixed diet as well (C3 and C4 plants).
2010, Table 1). The compilation of these dates reveals that this species lived in the BIR during the upper Pleistocene, 27–15 ka (Table 2). The age assigned to the N. platensis samples (Table 1) varied from 16,800–17,380 cal yr BP (13,980 ± 40 14C yr BP, UGAMS 4938) to 21,180–21,550 cal yr BP (17,910 ± 50 14C yr BP, UGAMS 4939). This is the species for which the largest number of specimens was previously dated (Table 2). Our results confirm the occurrence of this species between 17 ka and 22 ka. When the results of all published dates are combined, the occurrence of this species is estimated between 71 ka and 10 ka (Table 2). The ages assigned to the material of T. platensis (Table 1) ranged between 11,400–11,750 cal yr BP (10,050±30 14C yr BP, UGAMS 4946) and 12,660–13,050 cal yr BP (10,970±30 14C yr BP, UGAMS 4944). These ages reinforce the occurrence of this species in the beginning of the Holocene in the BIR as shown by Ribeiro et al. (in press; Table 2). These results combined with others from previous dating analyses indicate the occurrence of this species between 50 ka and 9 ka (Dantas et al., 2011; Ribeiro et al., in press; Table 2). Discussion Available chronological data (e.g. Auler et al., 2006; Dantas et al., 2011; Ribeiro et al., in press) indicated that E. laurillardi, N. platensis and T. platensis were present in the BIR during a long period of humidity at the end of the Pleistocene, between 40 ka and 10 ka. During this period the rainforests expanded (Behling et al., 2000; Auler and Smart, 2001; Sifeddine et al., 2003; Barreto, 2010), possibly providing a connection between the Atlantic forest and the Amazon rainforest. Although some pollen data for the dry forests (e.g. De Oliveira et al., 1999) and fossil leaves for the Atlantic forest of the BIR (e.g. Souza-Lima and Farias, 2008) pointed to a Pleistocene age, it is uncertain how these biomes were distributed in the BIR during the end of the Pleistocene. Due to this uncertainty, maps of potential distribution of the Atlantic forest (Carnaval and Moritz, 2008) and of the dry forests (savannah or steppic savannah; Werneck et al., 2011) comprising a period of 21 ka (Fig. 1) were used in order to observe the distribution of the studied fauna in relation to the biomes. We verified that the studied taxa were present both in open and closed environments. The resulting 13C data were grouped into three sub-regions: A (Rio Grande do Norte); B (Alagoas, Sergipe and north of Bahia); and C (south of Bahia). We considered that these species had the same diet in open environments, while in closed environments they showed differences, ranging from mixed feeders to exclusive C3 plants feeders (Table 1; Fig. 2). With regard to the 13C data, both ANOVA (E. laurillardi, Fobs =16.11, P=0.0029; N. platensis, Fobs =19.60, P=0.0018; T. platensis, Fobs = 10.77, P=0.0058) and non-parametric Kruskal–Wallis tests (E. laurillardi, Hobs =7.02, P=0.0298; T. platensis, Hobs =7.09, P=0.0288) indicate
Table 2 Compilation of the geochronological data for the species Eremotherium laurillardi, Notiomastodon platensis and Toxodon platensis found in fossiliferous deposits (“tanks” and caves) in the Brazilian Intertropical Region. Species
Age, ka 10−15 15−20 20−25 25−30 30−35 35−40 40−45 45−50 50−55 55−60 60−65
Radiocarbon dating The 14C dating analyses were performed using AMS for the E. laurillardi samples (Table 1) from the municipalities of Poço Redondo/SE and Currais Novos/RN. The results were, respectively, 26,690–27,690 cal yr BP (22,240 ± 50 14C yr BP, UGAMS 4932) and 18,580–18,850 cal yr BP (15,490 ±40 14C yr BP, UGAMS 4935). The age assigned for the sample of Sergipe state is the oldest reported for this species, whereas the age assigned to the material from Rio Grande do Norte is similar to the age obtained in two previous analyses using different techniques (Auler et al., 2006, U 238/Th230, 15 ka; Drefahl,
63
(1,2,3)
E. laurillardi
N. platensis
(4)
T. platensis
(3, 8, 9)
(1)
(3)
(3)
(3)
(5)
(5,6)
(4)
(8)
(6)
(7)
(6)
Auler et al. (2006), (2)Drefahl (2010), (3)Our data, (4)Oliveira et al. (2010), Kinoshita et al. (2005), (6)Dantas et al. (2011), (7)Kinoshita et al. (2008), (8) Ribeiro et al. (in press), (9)Neves et al. (2007). (5)
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both dental microwear analyses and tooth calculus suggested that N. platensis had the same type of diet, revealing that the same environmental conditions were present at the localities of Toca do Gordo do Garrincho/PI, Água de Araxá/MG, and São José do Itaboraí/RJ (Fig. 1). Conclusions
Figure 2. Tooth enamel carbon isotope (13C) values for the species analyzed in this study.
statistically significant differences among the three geographic samples. The only exception was the Kruskal–Wallis tests for N. platensis which indicated the same diet in all sub-regions. Between the latitudes 6°S to 9°S, there is a wide area (sub-region A, Fig. 1) in which the dry forests seemed to be predominant, most probably Caatinga vegetation (Behling et al., 2000; Werneck et al., 2011). The material concerning the three species which were collected in Rio Grande do Norte gives δ13C values that indicate a diet based exclusively on C4 grasses (Table 1). It is possible that in this kind of environment these species had a high competition for resources since they shared similar niches. South of latitude 9°S, in the region of Alagoas, Sergipe and northern of Bahia (sub-region B, Fig. 1), N. platensis had the same diet based exclusively on C4 grasses, which indicates that this was perhaps its predominant diet (Table 1), while E. laurillardi and T. platensis stopped feeding exclusively on C4 grasses and start browsing on C3 plants, thus becoming generalists (Table 1). The exclusive C3 plant-feeder value found in a sample from Alagoas for E. laurillardi (δ13C = −12.00‰, Silva, 2009) can be explained as a migrant specimen which came from Bahia. We infer that these C3 values are not from grasses, because a similar isotopic signal of C3 grass and browse plants occurs only at high latitudes (>35°S) or at high elevations (>3000 m) (MacFadden, 2005), which are not characteristic of our area of study. The vegetation in this region (sub-region B, Fig. 1) during this period is interpreted as a mosaic of dry forests (steppic savannah) and rainforests (Atlantic forest), where the species could occupy different niches and consequently reduce the competition for resources. In most of Bahia state (except for the northern region), and perhaps Minas Gerais, Piauí and Rio de Janeiro states, there would be the predominance of the Atlantic forest (Sub-region C, Fig. 1; Carnaval and Moritz, 2008), comprising a more closed area than found between latitudes 6°S and 10°S. Drefahl (2010) presented 13C data concerning E. laurillardi (Table 1) in this region, suggesting that in closed environments the diet of this species consisted exclusively in C3 plants. The fruits would be one of its main sources of food, thus the taxon is pointed as one of the main dispersal vectors of different botanic species (Guimarães et al., 2008). The data available for T. platensis and N. platensis pointed that in more closed environments these species fed more in C3 brows plant than in C4 grasses, tending to be exclusive C3 plant feeder (Table 1). Other evidence also supports this hypothesis. For example, the 13C data indicate the same type of diet for the fossil material related to these species. The material was found in a forest environment of the Amazon basin and its age ranged from 38.5 to 15 ka (Rossetti et al., 2004; MacFadden, 2005). Besides, Asevedo et al. (2011a,b) through
The fauna composed of the populations of E. laurillardi, N. platensis and T. platensis shows different diets throughout the Brazilian Intertropical Region, varying from exclusively grass feeders to mixed feeders. Thus, this fauna should not be used as an indicator of open environments, as Rossetti et al. (2004) previously stated. In a more closed environment these species tended to feed more on C3 plants, while in open area environments these species fed on C4 plants. In the latter, these species probably had a major competition for resources, which led them to have a population below its ideal number. Based on the carbon isotopic analysis, we considered that the ideal habitat for these species to be a mixed environment of Atlantic and dry tropical forest, since they presented different kinds of diet, which should decrease the competition for resources, and, maybe, allowed them to reach the ideal number of individuals for its populations. Acknowledgment We thank CAPES for the doutorament (doctoral) scholarship given to the first author, and FAPEMIG and USFISH for resources that helped with fields and the analysis. We thank Priscila Torres and Ale Boss for the English review of the manuscript, Adriana Bocchiglieri for the help in the statistical analyses, and anonymous reviewers whose corrections and suggestions improved the quality of this manuscript. References Asevedo, L., Winck, G.R., Mothé, D., Avilla, L.S., 2011a. Ancient diet of the Pleistocene gomphothere Notiomastodon platensis (Mammalia, Proboscidea, Gomphotheriidae) from lowland mid-latitudes of South America: stereomicrowear and tooth calculus analyses combined. Quaternary International http://dx.doi.org/10.1016/j.quaint. 2011.08.037. Asevedo, L., Oliveira, G.F. de, Avilla, L.S., Oliveira, E., Mothé, D., Winck, G.R., 2011b. Reconstrução da paleodieta de Notiomastodon platensis (Gomphotheriidae: Proboscidea: Mammalia) via análises de microdesgaste e cálculo dentário. Boletim de Resumos, Paleo2011, Alegre, Espírito Santo. Auler, A.S., Smart, P.L., 2001. Late Quaternary paleoclimate in semiarid northeastern Brazil from U-series dating of travertine and water-table speleothems. Quaternary Research 55, 159–167 http://dx.doi.org/10.1006/qres.2000.2213. Auler, A.S., Piló, L.B., Smart, P.L., Wang, X., Hoffmann, D., Richards, D.A., Edwards, R.L., Neves, W.A., Cheng, H., 2006. U-series dating and taphonomy of Quaternary vertebrates from Brazilian caves. Palaeogeography, Palaeoclimatology, Palaeoecology 240, 508–522 http://dx.doi.org/10.1016/j.palaeo.2006.03.002. Bargo, M.S., De Iuliis, G., Vizcaíno, S.F., 2006. Hypsodonty in Pleistocene ground sloths. Acta Palaeontolica Polonica 51 (1), 53–61. Barreto, E.A. de S., 2010. Reconstituição da pluviosidade da Chapada Diamantina (BA) durante o Quaternário tardio através de registros isotópicos (O e C) em estalagmites. Programa de Pós-graduação em Geoquímica e Geotectônica, Universidade de São Paulo, Dissertação de Mestrado, 133 pp. Behling, H., Arz, H.W., Tzold, J.R.P., Wefer, G., 2000. Late Quaternary vegetational and climate dynamics in northeastern Brazil, inferences from marine core GeoB 3104-1. Quaternary Science Reviews 19, 981–994. Carnaval, A.C., Moritz, G., 2008. Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic Forest. Journal of Biogeography 35, 1187–1201 http://dx.doi.org/10.1111/j.1365-2699.2007.01870.x. Cartelle, C., 1999. Pleistocene mammals of the Cerrado and Caatinga of Brazil. In: Eisenberg, J.F., Redford, K.H. (Eds.), Mammals of the Neotropics. The University of Chicago Press, pp. 27–46. Cerling, T.E., Harris, J.M., 1999. Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120, 347–363. Dantas, M.A.T., Porpino, K.deO., Bauermann, S.G., Prata, A.P. do N., Cozzuol, M.A., Kinoshita, A., Barbosa, J.H.O., Baffa, O., 2011. Megafauna do Pleistoceno superior de Sergipe, Brasil: registros taxonômicos e cronológicos. Revista Brasileira de Paleontologia 14 (3), 311–320 http://dx.doi.org/10.4072/rbp. 2011.3.10. De Oliveira, P.E., Barreto, A.M.F., Suguio, K., 1999. Late Pleistocene/Holocene climatic and vegetational history of the Brazilian Caatinga: the fossil dunes of the middle São Francisco river. Palaeogeography, Palaeoclimatology, Palaeoecology 152, 319–337.
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